Fly's courtship sheds light on the formation of innate behaviors

By studying how genes influence the development and use of neural circuits that control a specific set of mating behaviors in the fruit fly, researchers have provided new insight into how instinctual behaviors – those that are not based on prior experience – arise in the developing nervous system. The work is reported by Jean-Christophe Billeter and other members of Stephen Goodwin's group at the University of Glasgow, along with research groups at Brandeis and California State University, and appears in the June 6th issue of Current Biology.

Instinctual behaviors, such as suckling in newborns, or the flight-fight response, are generally seen as subconscious drives underlying the actions of humans and other animals. Yet the manner by which these innate behaviours are hard-wired into our brains remains obscure.

In their new work, the researchers set out to address this question using mutations that perturb the stereotypical male courtship behavior of the fruit fly Drosophila melanogaster. The male fly, in its attempt to mate, will perform a series of complex behaviours – including following females, singing, licking, and tapping – that are not based on the fly's past experience. One gene, fruitless, has been shown to be pivotal to the emergence of these stereotypical behaviours. Fruitless is known to generate a variety of similar but functionally different proteins, some of which are exclusively expressed in male flies.

Using a mutant that specifically disrupts one form of the Fruitless protein, the researchers showed that the male fly's sexual behavior is not a closed neural circuit, but rather a series of independent but interlinked steps that are regulated to have an additive effect on the success of the courtship behavior as a whole.

Studying various mutants, the researchers were able to uncouple the later steps of copulation from the earlier courtship steps, assigning specific populations of neurons to the behaviors involved, and thereby going a long way in describing how the neural code for these behaviors is formulated in the developing fly's brain. This work, in conjunction with other studies performed by these and other research groups in recent years, shows how fundamentally important one gene can be to effecting a behavior, and how that behavior can be altered (and potentially evolve) as the gene itself is affected by external cues, by interactions with other genes, and by the organism's neuronal environments.

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The researchers include Jean-Christophe Billeter, Anthony J. Dornan, Michael Richardson, and Stephen F. Goodwin of the University of Glasgow in Glasgow, United Kingdom; Adriana Villella of Brandeis University in Waltham, MA; Jane B. Allendorfer and Donald A. Gailey of California State University in Hayward, CA.

The research was supported by J.-C.B., A.J.D., M.R., and S.F.G. were supported by grants from the Wellcome Trust and the Royal Society. D.A.G. was supported by National Institutes of Health (NIH) Minority Biomedical Research Support Grant GM48135. A.V. was supported by U.S. NIH grants GM-21473 and NS-33352 to Jeffrey C. Hall (Brandeis University).

Billeter et al.: "Isoform-Specific Control of Male Neuronal Differentiation and Behavior in Drosophila by the fruitless Gene." Publishing in Current Biology 16, 1063–1076, June 6, 2006 DOI 10.1016/j.cub.2006.04.039 www.current-biology.com

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